Abstract
Object
As a broad-spectrum fluoroquinolone antibiotic drug, ciprofloxacin (CIP) is frequently used in the treatment of a wide variety of infections. However, the residues of this antibiotic pose a big threat to the aquatic environment and human health. In this research, Lactobacillus reuteri WQ-Y1 with CIP degradation ability was screened and identified.
Results
L. reuteri WQ-Y1 with a degradation rate of 65.1% for 4 µg mL−1 CIP was screened from 17 lactic acid bacteria (LAB), and cytochrome P450 enzyme was confirmed to promote the degradation of CIP by L. reuteri WQ-Y1. Meanwhile, the CIP degradation rate were also higher in 48 h’ culture time when co-cultured with 1 mg/mL of glucose in the culture media. Furthermore, result also proved that fluoroquinolone antibiotics with the similar piperazine ring structures could be degraded by L. reuteri WQ-Y1.
Conclusions
L. reuteri WQ-Y1 could degrade fluoroquinolone antibiotics with the similar piperazine ring structure. However, future work still needs to be done on the confirmation of the key enzymes in the cytochrome P450 enzymes family in the biodegradation.
Graphic Abstract
The isolated ciprofloxacin-degrading strain L. reuteri WQ-Y1 had a CIP degradation rate of 65.1% at 24 hours, and one biodegradation metabolite was identified and proved to be an important metabolite of CIP from cytochrome P450 enzymes family hydrolysis with UPLC-MS/MS spectrograms approach.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adjei MD, Heinze TM, Deck J, Freeman JP, Williams AJ, Sutherland JB (2006) Transformation of the antibacterial agent norfloxacin by environmental mycobacteria. Appl Environ Microbiol 72:5790–5793. https://doi.org/10.1128/AEM.03032-05
Adjei MD, Deck J, Heinze TM, Freeman JP, Williams AJ, Sutherland JB (2007) Identification of metabolites produced from N-phenylpiperazine by Mycobacterium spp. J Ind Microbiol Biotechnol 34:219–224. https://doi.org/10.1007/s10295-006-0189-x
Amorim CL, Moreira IS, Maia AS, Tiritan ME, Castro PML (2014) Biodegradation of ofloxacin, norfloxacin, and ciprofloxacin as single and mixed substrates by Labrys portucalensis F11. Appl Microbiol Biotechnol 98:3181–3190. https://doi.org/10.1007/s00253-013-5333-8
Ardebili A, Talebi M, Azimi L, Rastegar LA (2014) Effect of efflux pump inhibitor carbonyl cyanide 3-chlorophenylhydrazone on the minimum inhibitory concentration of ciprofloxacin in Acinetobacter baumannii clinical isolates. Jundishapur J Microb 7:e8691. https://doi.org/10.5812/jjm.8691
Borthakur A, Gill RK, Tyagi S, Koutsouris A, Alrefai WA, Hecht GA, Ramaswamy K, Dudeja PK (2008) The probiotic Lactobacillus acidophilus stimulates chloride/hydroxyl exchange activity in human intestinal epithelial cells. J Nutr 138:1355–1359. https://doi.org/10.1093/jn/138.7.1355
Boxall ABA, Kolpin DW, Halling-S Rensen B, Tolls J (2003) Peer reviewed: are veterinary medicines causing environmental risks? Environ Sci Technol 37:286A-294A. https://doi.org/10.1021/es032519b
Dai Y, Li N, Zhao Q, Xie S (2015) Bioremediation using Novosphingobium strain DY4 for 2,4-dichlorophenoxyacetic acid-contaminated soil and impact on microbial community structure. Biodegradation 26:161–170. https://doi.org/10.1007/s10532-015-9724-7
Gobel A, Thomsen A, Mcardell CS, Joss AA, Giger W (2005) Occurrence and sorption behavior of sulfonamides, macrolides, and trimethoprim in activated sludge treatment. Environ Sci Technol 39:3981–3989. https://doi.org/10.1021/es048550a
Gu R, Yang Z, Li Z, Chen S, Luo Z (2008) Probiotic properties of lactic acid bacteria isolated from stool samples of longevous people in regions of Hotan, Xinjiang and Bama, Guangxi, China. Anaerobe 14:313–317. https://doi.org/10.1016/j.anaerobe.2008.06.001
Ha NR, Jung IP, La IJ, Jung HS, Yoon MY (2017) Ultra-sensitive detection of kanamycin for food safety using a reduced graphene oxide-based fluorescent aptasensor. Sci Rep-UK 7:40305. https://doi.org/10.1038/srep40305
Han Y, Yang L, Chen X, Cai Y, Zhang X, Qian M, Cao G, Shen G (2020) Removal of veterinary antibiotics from swine wastewater using anaerobic and aerobic biodegradation. Sci Total Environ 709:136094. https://doi.org/10.1016/j.scitotenv.2019.136094
Hernando MD, Mezcua M, Fernandezalba AR, Barcelo D (2006) Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta 69:334–342. https://doi.org/10.1016/j.talanta.2005.09.037
Jia Y, Khanal SK, Shu H, Zhang H, Chen G, Lu H (2018) Ciprofloxacin degradation in anaerobic sulfate-reducing bacteria (SRB) sludge system: mechanism and pathways. Water Res 136:64–74. https://doi.org/10.1016/j.watres.2018.02.057
Johnson AC, Keller V, Dumont E, Sumpter JP (2015) Assessing the concentrations and risks of toxicity from the antibiotics ciprofloxacin, sulfamethoxazole, trimethoprim and erythromycin in European rivers. Sci Total Environ 511:747–755. https://doi.org/10.1016/j.scitotenv.2014.12.055
Kumar K, Gupta SC, Chander Y, Singh AK (2005) Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron 87:1–54. https://doi.org/10.1016/S0065-2113(05)87001-4
Li B, Zhang T (2010) Biodegradation and adsorption of antibiotics in the activated sludge process. Environ Sci Technol 44:3468–3473. https://doi.org/10.1021/es903490h
Liao X, Chen C, Zhang J, Dai Y, Zhang X, Xie S (2015) Dimethylamine biodegradation by mixed culture enriched from drinking water biofilter. Chemosphere 119:935–940. https://doi.org/10.1016/j.chemosphere.2014.09.020
Liao X, Li B, Zou R, Xie S, Yuan B (2016) Antibiotic sulfanilamide biodegradation by acclimated microbial populations. Appl Microbiol Biot 100:2439–2447. https://doi.org/10.1007/s00253-015-7133-9
Maia AS, Ribeiro AR, Amorim CL, Barreiro JC, Cass QB, Castro PML, Tiritan ME (2014) Degradation of fluoroquinolone antibiotics and identification of metabolites/transformation products by liquid chromatography–tandem mass spectrometry. J Chromatogr A 1333:87–98. https://doi.org/10.1016/j.chroma.2014.01.069
Martínez J (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367. https://doi.org/10.1126/science.1159483
Müller E, Schüssler W, Horn H, Lemmer H (2013) Aerobic biodegradation of the sulfonamide antibiotic sulfamethoxazole by activated sludge applied as co-substrate and sole carbon and nitrogen source. Chemosphere 92:969–978. https://doi.org/10.1016/j.chemosphere.2013.02.070
Pan LJ, Tang XD, Li CX, Yu GW, Wang Y (2017) Biodegradation of sulfamethazine by an isolated Thermophile–geobacillus sp. s-07. World J Microb Biotechnol 33(5):85. https://doi.org/10.1007/s11274-017-2245-2
Pan LJ, Li J, Li CX, Tang X, Yu GW, Wang Y (2018) Study of ciprofloxacin biodegradation by a Thermus spp. isolated from pharmaceutical sludge. J Hazard Mater 343:59–67. https://doi.org/10.1016/j.jhazmat.2017.09.009
Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC (2006) Prevalence in the united states of aac(6")-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Ch 50:2955–3953. https://doi.org/10.1128/AAC.00915-06
Patel JB (2015) Performance standards for antimicrobial susceptibility testing: twenty-fourth informational supplement. Clinical and Laboratory Standards Institute, Wayne, PA
Peng X, Qu X, Luo W, Jia X (2014) Co-metabolic degradation of tetrabromobisphenol A by novel strains of Pseudomonas sp. and Streptococcus sp. Bioresour Technol 169:271–276. https://doi.org/10.1016/j.biortech.2014.07.002
Prieto A, Möder M, Rodil R, Adrian L, Marco-Urrea E (2011) Degradation of the antibiotics norfloxacin and ciprofloxacin by a white-rot fungus and identification of degradation products. Bioresour Technol 102:10987–10995. https://doi.org/10.1016/j.biortech.2011.08.055
Samanidou VF, Demetriou CE, Papadoyannis IN (2003) Direct determination of four fluoroquinolones, enoxacin, norfloxacin, ofloxacin, and ciprofloxacin, in pharmaceuticals and blood serum by HPLC. Anal Bioanal Chem 375:623–629. https://doi.org/10.1007/s00216-003-1749-9
Sivakumar S, Anitha P, Ramesh B, Suresh G (2017) Analysis of EAWAG-BBD pathway prediction system for the identification of malathion degrading microbes. Bioinformation 13:73–77. https://doi.org/10.6026/97320630013073
Wang Z, Yang Y, Sun W, Xie S (2014) Biodegradation of nonylphenol by two alphaproteobacterial strains in liquid culture and sediment microcosm. Int Biodeter Biodegr 92:1–5. https://doi.org/10.1016/j.ibiod.2014.04.004
Wetzstein H, Schneider J, Karl W (2006) Patterns of metabolites produced from the fluoroquinolone enrofloxacin by basidiomycetes indigenous to agricultural sites. Appl Microbiol Biotechnol 71:90–100. https://doi.org/10.1007/s00253-005-0178-4
Wetzstein H, Schneider J, Karl W (2012) Metabolite proving fungal cleavage of the aromatic core part of a fluoroquinolone antibiotic. AMB Express 2:3. https://doi.org/10.1186/2191-0855-2-3
Xiong J, Kurade MB, Kim JR, Roh H, Jeon B (2017) Ciprofloxacin toxicity and its co-metabolic removal by a freshwater microalga Chlamydomonas mexicana. J Hazard Mater 323:212–219. https://doi.org/10.1016/j.jhazmat.2016.04.073
Yolanda P, Vicente A (2006) Fluoroquinolones in soil—risks and challenges. Anal Bioanal Chem 387:1287–1299. https://doi.org/10.1007/s00216-006-0843-1
Acknowledgements
This work was supported by the National Natural Science Foundation of China (32072192, 31671869, 31901668), Key Research and Development Project of Zhejiang Province (2020C02042), the Natural Science Foundation of Zhejiang Province (LY19C200005), the Open Project Program of State Key Laboratory of Dairy Biotechnology (No. SKLDB2020-007) and the K. C. Wong Magna Fund in Ningbo University.
Supplementary information
SupplementaryFigure S1—The degradation rate of CIP by 17 strains of LAB with different MIC at 48 h.
Author information
Authors and Affiliations
Contributions
CXQ performed the ciprofloxacin-degrading strains screening in this study, ZW and DDP contributed to the conception of the study, ZDC performed the cytochrome P450 enzymes activity analysis, XTL helped perform the analysis with constructive discussions, CXQ was a major contributor in writing the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Qu, C., Wu, Z., Pan, D. et al. Characterization of Lactobacillus reuteri WQ-Y1 with the ciprofloxacin degradation ability. Biotechnol Lett 43, 855–864 (2021). https://doi.org/10.1007/s10529-020-03068-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10529-020-03068-9